A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene

Abstract

Zymoseptoria tritici is the causal agent of Septoria tritici blotch, a major pathogen of wheat globally and the most damaging pathogen of wheat in Europe. A gene-for-gene (GFG) interaction between Z. tritici and wheat cultivars carrying the Stb6 resistance gene has been postulated for many years, but the genes have not been identified. We identified AvrStb6 by combining quantitative trait locus mapping in a cross between two Swiss strains with a genome-wide association study using a natural population of c. 100 strains from France. We functionally validated AvrStb6 using ectopic transformations. AvrStb6 encodes a small, cysteine-rich, secreted protein that produces an avirulence phenotype on wheat cultivars carrying the Stb6 resistance gene. We found 16 nonsynonymous single nucleotide polymorphisms among the tested strains, indicating that AvrStb6 is evolving very rapidly. AvrStb6 is located in a highly polymorphic subtelomeric region and is surrounded by transposable elements, which may facilitate its rapid evolution to overcome Stb6 resistance. AvrStb6 is the first avirulence gene to be functionally validated in Z. tritici, contributing to our understanding of avirulence in apoplastic pathogens and the mechanisms underlying GFG interactions between Z. tritici and wheat.

A fungal avirulence factor encoded in a highly plastic genomic region triggers partial resistance to septoria tritici blotch

“…Two highly conserved lysin motif (LysM) effectors, Mg1LysM and Mg3LysM, prevent fungal recognition and shield the fungal cell wall from degradation by host hydrolytic enzymes (Marshall et al ., 2011). The other known effectors of Z. tritici , Zt80707, AvrStb6 and Zt_8_609, are rapidly evolving small secreted proteins (Poppe et al ., 2015; Hartmann et al ., 2017; Zhong et al ., 2017; Kema et al ., 2018). The latter two were identified because they are specifically recognised by certain wheat cultivars, and they were found to be located in transposable element‐rich genomic regions (Brading et al ., 2002; Hartmann et al ., 2017; Zhong et al ., 2017).…”

“…The other known effectors of Z. tritici , Zt80707, AvrStb6 and Zt_8_609, are rapidly evolving small secreted proteins (Poppe et al ., 2015; Hartmann et al ., 2017; Zhong et al ., 2017; Kema et al ., 2018). The latter two were identified because they are specifically recognised by certain wheat cultivars, and they were found to be located in transposable element‐rich genomic regions (Brading et al ., 2002; Hartmann et al ., 2017; Zhong et al ., 2017). AvrStb6 is recognised by the resistance protein Stb6 in a gene‐for‐gene interaction that leads to a strong resistance response, completely blocking the progression of the infection (Kema et al ., 2000, 2018; Brading et al ., 2002; Saintenac et al ., 2018).…”

Durum wheat and septoria tritici blotch: genes and prospects for breeding

“…We currently cannot explain these differences, but the data were clearly independently collected during different experimental conditions, which would confirm that Z. tritici is very sensitive to environmental fluctuations (Ben M'Barek et al 2015). However, notwithstanding these differences, AvrStb6 -as a classical avirulence effector -determines the outcome of the interaction as shown by the current data and by previous data Zhong et al 2017). …”

“…Similarly, the broad efficacy of Stb22q is demonstrated for P, but not for N. We do not know why durum wheats exhibit extensive necrosis as a result of Z. tritici infections, but the current data also demonstrate that N and P are under different genetic control ). The recent cloning of AvrStb6 Zhong et al 2017); will likely help to resolve more mechanistic details of Z.…”

“…The (a)virulence gene was subsequently mapped on the distal part of chromosome 5, and cosegregates with the genomic region responsible for the host specificity, widely reported in a range of studies (Eyal et al 1973;Mirzadi Gohari et al 2015;Van Ginkel and Scharen 1988;Ware 2006). Albeit early reported, host specificity and cultivar specificity in the Z. tritici pathosystem remain inscrutable as so far only genes controlling cultivar specificity have been identified (this thesis; (Zhong et al 2017)). Nevertheless, whilst the reported GFG model has greatly enhanced gene postulation in bread wheat resulting into the identification of 21 Stb major resistance genes , the dichotomy in Z. tritici is a burden for gene postulation in durum wheat, hampering its improvement for STB resistance.…”